Erythmelus klopomor: First steps toward classical biological control of the oak lace bug Corythucha arcuata, a dangerous invader in the European oak forests

Erythmelus klopomor: First steps toward classical biological control of the oak lace bug Corythucha arcuata, a dangerous invader in the European oak forests | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Erythmelus klopomor: First steps toward classical biological control of the oak lace bug Corythucha arcuata, a dangerous invader in the European oak forests MÁRTON J. PAULIN, GEORGE MELIKA, SERGUEI TRIAPITSYN, DAVID BECHTEL, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5795762/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The North American oak lace bug (OLB), Corythucha arcuata (Say, 1832) (Hemiptera: Tingidae), is a very dangerous invasive pest of European oaks ( Quercus spp., Fagaceae). It was first detected in Europe in 2000 and currently occurs in 26 countries in the Palearctic region. Most Eurasian deciduous oaks are suitable host plants, therefore about 30 million hectares of oak dominated forests in Europe can facilitate its rapid spread. Its negative effects can be very diverse: decreasing photosynthetic activity, deteriorating health, decreasing acorn yield, negative effect on other oak herbivorous insects, and more. One of the main reasons for its rapid expansion is that native European predators, parasitoids and insect pathogens are unable to control it. The only feasible control option is a classical biological control program, the essence of which is to find and introduce a preferably specialist regulatory species that is effective in the pest’s native range. In July 2023 and in 2024, we collected oak leaves with OLB eggs from different locations in six states of the United States of America. All emerged egg parasitoids were preserved for later identification. Our initial observation was that collecting OLB eggs in the field proved to be more challenging than we first assumed. Overall, 23.7% of the samples contained parasitoids, with the average parasitism of 14.5%. Up to this point results indicate that the fairyfly Erythmelus klopomor Triapitsyn, 2007 (Hymenoptera: Mymaridae) is the only known egg parasitoid of OLB. Its host range is restricted to lace bugs, mainly Corythucha spp., and C. arcuata seems to be its preferred host. Our conclusion is that E. klopomor is a promising and only (at least so far) candidate for a classical biological control program, but further research efforts are unavoidable to clarify its life history parameters and minimize the risk of unintended non-target effects prior to a potential deliberate introduction to Europe. Oak lace bug Erythmelus klopomor Biological invasion Classical biological control Egg parasitoid Figures Figure 1 Key Message The invasive Corythucha arcuata is a very dangerous pest of the European oak dominated forests Native enemies in Europe have no regulatory potential against C. arcuata Only a classical biological control program seems to be a feasible solution So far E. klopomor seems to be the only specialist parasitoid against C. arcuata Introduction Alien insect species can pose serious threats to various ecosystems worldwide (Roques 2010; Csóka et al. 2017; Liebhold et al. 2017). While some of them do not have an evident impact on the newly colonized ecosystems, others may become invasive, rapidly expanding their range and imposing severe pressures on the novel habitats (Mollot et al. 2017; Blackburn et al. 2019; Haubrock et al. 2021). Whether a non-native species can become invasive is influenced by several intrinsic, species-specific traits as well as by external biotic and abiotic factors. An important, often appearing factor is the lack of regulatory effects by natural enemies; the so-called escape-from-enemy or enemy-release hypothesis (Brockerhoff et al. 2006; Brockerhoff & Liebhold 2017; Firlej et al. 2012). The North American oak lace bug (OLB), Corythucha arcuata (Say) (Hemiptera: Tingidae) was first found in Europe in northern Italy in 2000 (Bernardinelli 2000), and up to 2024 it was recorded in 24 European and 1 Asian countries (Paulin et al. 2023; Ciceu et al. 2024). Almost all Eurasian deciduous oak species are suitable hosts, and it can also feed on many other woody plants (Csóka et al. 2019). More than 30 million hectares of oak forests in Europe provide suitable hosts for the OLB, meaning that the lack of suitable hosts will not restrict its further spread (Csóka et al. 2019; Csepelényi et al. 2017a; Paulin et al. 2020). OLB is also a typical “hitchhiker”, and its long-distance spread is supported by traffic. With this human-mediated help, it can overcome long distances and natural barriers within a short time. Also, after assessing the intensity of infestation on several pure and mixed oak stands in five countries, the conclusion was that mixed stands (while they mitigate OLB damage) do not prevent severe infestation (Hoch et al. 2024). Climate may also have a very significant influence on the establishment, spread and population dynamics of an alien invasive species. Our field survey on the overwintering mortality (Csepelényi et al. 2017b; Paulin et al. 2019) proved that the overwintering adults survived even relatively cold winters with ca. 50% or even less mortality. Lab experiments also proved that while OLB is a freeze-avoidant species, some adults may survive temperatures as low as -29°C (Paulin et al. 2021). Therefore, it is unlikely that low winter temperatures would significantly reduce spread of the OLB. Detailed studies on the long-term impact of this species are not yet available but there are many good reasons to assume that it poses multiple threats to oaks and oak ecosystems (Paulin et al. 2020, Kern et al. 2021). Heavy infestation of OLB on oaks may cause yellow-grey discoloration throughout the foliage by the second part of the vegetation season, sometimes even as early as late June (Csepelényi et al. 2017a; Paulin et al. 2020). Drone, aerial and even space images (MODIS, Sentinel, Google Earth, etc.) have been used to detect severe infestations in several countries (Neimorovets et al. 2017; Kern et al. 2021). According to a Serbian study, the photosynthetic activity on heavily infested leaves decreased by 58.8% (Nikolić et al. 2019). Using MODIS data, the damage attributed to the OLB is also significant: NDVI decrease down to -14.5% in pure pedunculate oak forests (Kern et al 2021). It is very unlikely that such an impact would not have severe long-term effects on the oaks’ nutrient and water flow. There is currently also no information on whether any oak pathogen present in these regions might potentially be vectored by OLB. It is yet unknown how several years of heavy OLB infestation will influence acorn crop, or what the effect on the oak herbivorous communities or other oak-associated species (like fungi or litter decomposers) will be. As the damage caused by OLB is more significant in the second half of the vegetation period, this influence can seriously harm oak specialist populations (Paulin et al 2020). Adding to this, it was recorded of the closely related sycamore lace bug, Corythucha ciliata (Say), that their feeding attempts cause painful inflammations on human skin (Dutto & Bertero 2013; Izri et al. 2015). Similar results about OLB have not yet been documented, but our own experiences proved that OLB can cause similar symptoms (Paulin et al. 2020). This kind of human/OLB interaction will become more frequent in the future, especially in parks, oak alleys in towns and private gardens with planted oaks. Based on current research results we found only a few species native in Europe which can be considered as occasional natural enemies of OLB. Most of the species recorded are generalists with negligible effect, such as Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) or Theridion pinastri L. Koch (Araneae: Theridiidae) (Paulin et al. 2020). There are also records of entomopathogenic fungi naturally infecting overwintering OLB (Kovač et al. 2020). However, none of the above-mentioned native species have any significant controlling effect on OLB. During 2019-2020, parasitoids of the invasive C. arcuata were studied in Bulgaria (Georgiev et al. 2024). Larvae were collected from European oak ( Quercus robur ) and Turkey oak ( Quercus cerris ) in five localities of the country. Five eulophid species (Hymenoptera: Eulophidae) were reported to be reared from the host larvae: Tamarixia pubescens (Nees), Elasmus sp., Minotetrastichus sp., Pnigalio sp. and Sympiesis sp. The impact of the parasitoids on the host number was reported to be very low (0.1-0.3%). However, Tamarixia pubescens is a parasitoid of psyllids (Hemiptera: Psylloidea); known to parasitize Trioza remota (Foerster) (Triozidae), which, at nymphal stage, is an oak obligate (Thunes et al. 2021). Elasmus spp. most often were recorded as parasitoids of Lepidoptera (Yefremova and Strakhova 2010); and Minotetrastichus sp., Pnigalio sp., Sympiesis sp. are known to parasitize various leaf miners (Boucek 1959; Zhu and Huang 2003; Japoshvili and Kostjukov 2017). Therefore, contamination of the samples (parasitoids emerging from other insects on or in the leaf samples in the rearing dishes) cannot be excluded, and, in fact, was almost certainly the case. Until proven otherwise by thorough experimental work, we do not consider these five species as being OLB parasitoids. In our opinion none of the native natural enemies (including pathogens) have any potential at regulating OLB in its invaded range in the Palearctic region. To control an insect pest, promising biological control candidates in its area of origin – usually parasitoids – often are chosen based on high observed parasitism levels (Hawkins et al. 1993). Such was the case with the chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) that has a strong negative effect on the growth of chestnut trees (Kato and Hijii 1997). A specialist parasitoid, Torymus sinensis Kamijo (Hymenoptera: Torymidae), was introduced in multiple countries against this gall wasp (Ferracini et al. 2017). Post-release studies have found T. sinensis to be its effective biological control agent (Matošević et al. 2016; Ferracini et al. 2017). Egg parasitoids of Tingidae have been discovered in the past, mostly when their effects were of economic importance. Such cases were the parasitoids of the Chrysanthemum lace bug, Corythucha marmorata (Uhler) (Puttler & Triapitsyn 2006; Triapitsyn et al. 2024); the avocado lace bug, Pseudacysta perseae (Heidemann) (Peña et al. 2009), and the OLB as well (Puttler et al. 2014). The subject of the latter was Erythmleus klopomor Triapitsyn (Hymenoptera: Mymaridae) which up to now is the only known parazitoid of OLB in its native range. Materials and Methods In the first half of July 2023, we collected oak leaves with OLB egg bunches from 13 different locations in five states of the USA (Fig. 1., Table 1.). Leaves collected were first observed, and only further processed, if we estimated the percentage of unhatched eggs to be high enough (above 80%). Leaf parts with egg bunches were cut, producing approximately 2 cm-by-2 cm pieces. These were then put into transparent 25 ml containers, with a piece of paper tissue, held at room temperature, and checked every 1-3 days for emergence of either egg parasitoids or host nymphs. Table 1 : Locations and dates of collection Site ID. Location Longitude Latitude Date of collection 1 Newark, DE 39.66227 -75.75012 2023.07.07 2 Allentown, PA 40.61206 -75.56745 2023.07.08 3 Kutztown, PA 40.51368 -75.78722 2023.07.09 4 Lewisburg, PA 40.98655 -76.93337 2023.07.10 5 Penn State U., PA 40.91094 -77.28275 2023.07.12 6 Morgantown, WV 40.80475 -77.86446 2023.07.13 7 Garards Fort, PA 39.65119 -79.98773 2023.07.13 8 Coonskin Park, WV 39.79613 -80.09182 2023.07.14 9 Little Creek Park, WV 38.38667 -81.57509 2023.07.15 10 Virginia Tech. U., VA 38.34115 -81.72315 2023.07.16 11 Pandapas Pond, VA 37.22500 -80.42691 2023.07.16 12 McCormick Farm, VA 37.28206 -80.46833 2023.07.17 13 Agricultural RS, MD 37.93275 -79.21297 2023.07.18 14 Knoxville, Tennessee 35.85089 -84.09388 2024.06.20. 2024.07.29. 2024.08.24. Another separate sampling was done in Knoxville, Tennessee between 2024.06.20. and 2024.08.24. This collection will in later tables be identified as sample number 14. Samples were collected at three different times from the same tree and were processed in a similar way. If a large percentage of unhatched eggs was found, the leaf parts with egg bunches were cut. These were then put into transparent plastic Petri dishes with a piece of paper tissue and sealed using Parafilm. Upon emergence, parasitoids emerged were collected and put into 2 ml Eppendorf tubes with 90% ethanol for later identification. Checking continued up to 39 days after collection. Individual eggs of bunches with parasitoids were also counted, to calculate parasitism rates for these samples. For the average rearing day count we used weighted arithmetic mean. Results Our initial observation was that collecting OLB eggs in the field proved to be more challenging than we first assumed. The abundance of OLB in its native range was magnitudes lower than what we have documented in Europe. On oaks that were in or close to natural habitats, we found only very few OLB-infested leaves. Our largest samples were collected in urban habitats or close to them, for example in university campuses or at roadsides. This supports our theory that one of the main factors for OLB’s success in its invaded range is the enemy free place. In our experience the ‘naïve host plant’ theory doesn’t hold because as Csóka et al. (2019) showed, that species from OLB’s native range were just as infected in the European sentinel gardens and arboreta, as in forests with European native oak species. In total during the two years of collecting, we visited 7 states in the USA, and from 14 locations we were able to collect a total of 423 individual egg masses, which contained above 95% unhatched eggs. Out of the 423 samples we have managed to rear parasitoids from 107 samples (Table 2). In the locations where the collected samples yielded no parasitoids, we were unable to collect more than 15 unhatched egg bunches. In the parasitized samples we counted 4569 oak lace bug eggs total, out of which we reared 721 parasitoids. The average mortality in the parasitized samples was between 3.6% and 18.3%, with the average of averages being 14.5%. The average rearing day count (days between collecting and emergence) ranged from 8.6 to 24.6 days, with the average of averages being 19.5 days. It is important to remark, that these rearing days are most likely overestimates, as checking did not occur daily and sometimes only dead E. klopomor specimens were found. Table 2 : Results of Erythmelus klopomor rearing (Abbreviations: ID.: Sample location ID from the previous table; SPL: Samples per location (pcs); SWP: Samples with parasitoids emerged (pcs); RP: Reared parasitoids in all samples (pcs); POLB: All OLB eggs in parasitised samples (pcs); ADTH: Avg. days to hatch after collecting; PSP: Percentage of samples parasitised; AEM: Avg. egg mortality in parasitized samples) ID. SPL SWP RP POLB ADTH PSP AEM 1 49 4 17 178 19.2 8.2% 9.6% 2 16 6 78 284 20.6 37.5% 27.5% 3 49 14 100 622 18.8 28.6% 16.1% 4 38 6 40 358 14.3 15.8% 11.2% 5 21 7 47 327 19.6 33.3% 14.4% 6 16 1 15 86 11.0 6.3% 17.4% 7 15 0 0 0 - - - 8 24 4 14 124 15.1 16.7% 11.3% 9 34 12 59 331 19.4 35.3% 17.8% 10 22 2 5 141 15.2 9.1% 3.6% 11 4 0 0 0 - - - 12 22 2 4 36 8.8 9.1% 11.1% 13 91 40 225 1443 18.9 44.0% 15.6% 14 22 9 103 639 24.6 40.9% 18.0% Overall 423 107 707 4569 19.5 23.7% 14.5% Even though the number of 2024 samples from Tennessee was relatively low, it is still important to analyze them separately as they were collected on three different dates (Table 3). Nine out of 22 samples from there contained parasitoids. For these we compared the percentage of samples parasitized and the average egg mortality. The former shows an increase if we compare only the first two collecting dates; and the second shows an increase throughout all three collecting dates. Table 3: Results of Erythmelus klopomor rearing in Tennessee in 2024 Date of collection Samples per location Samples with parasitoids emerged Percentage of samples parasitized Avg. egg mortality in parasitized samples 2024.06.20. 10 3 30.0% 5.5% 2024.07.29. 8 5 62.5% 25.6% 2024.08.24. 4 1 25.0% 26.9% Discussion Egg parasitoids, by definition, both attack and complete their development within a host egg (Mills 1994). The notion of killing a pest before it can hatch and cause significant damage to the host is appealing and is an important contributing factor for the usage of egg parasitoids in biological control and integrated pest management (Hassan 1993). In the context of classical biological control introductions, mymarid introductions have provided a number of spectacular results, and such opportunities should always be considered for new invasive pests, with particular emphasis on cicadellids and curculionids (Mills 2009). The success of augmentative biological control with egg parasitoids has been mixed, which highlights the need to know more about their ecology and behavior (Mills 2009). For example, to fully understand the impact that egg parasitoids have on host populations, all forms of parasitoid-induced mortality need to be considered – for example, host eggs that have been parasitized, but from which neither parasitoids nor the hosts have emerged. Our findings add five new states (Delaware, Pennsylvania, Tennessee, Virginia and West Virginia) in the USA to the previously known range of E. klopomor . Puttler et al. (2014) reported it from Florida, Illinois, Missouri, North Carolina and Maryland. Although average temperature in these states is somewhat similar to temperature in the southern parts of Europe, there are plans to study distribution of this parasitoid in the northern regions of the United States. It is also important to acknowledge that most of our data is based on estimates. During the 2023 sampling we estimated the amount of unhatched OLB eggs in all samples to be above 80%, meaning there may have been eggs from which parasitoids could have already hatched. Also, in both years, after we completed rearing from the samples, we were unable to determine if there were any eggs (in any of the samples) which were unhatched. These eggs could have possibly contained E. klopomor larvae, which were unable to develop for some reason. Therefore, both the percentage of parasitized samples and the average egg mortality caused by E. klopomor were probably higher than what we have documented here. Although the parasitism and mortality rates we documented seem to be low, it is important to note that most of these samplings were done in the first part of the vegetation period. Our theory (supported by our preliminary results) is that the rate of parasitism rises throughout the vegetative season, which is why it is capable of controlling OLB. The description of E. klopomor’ s biology by Puttler et al. (2014) affirms this by reporting that the life cycle from egg to adult ranged from 11–17 days. This means that its fast development enables it to “catch up” to the OLB’s multiple overlapping generations, and efficiently reduces the host’s numbers in the later months of the vegetation period. Further studies of this parasitoid are planned to understand its ecology better. We plan to study its overwintering habits, to ensure that it is capable of surviving in a novel environment. Studying host specificity and potential non-target effects is also a crucial point of this species’ suitability as a classical biological control agent, especially considering that in its native range E. klopomor was reported from several tingid species, mainly Corythucha spp. (Triapitsyn et al. 2007; Peña et al. 2009; Puttler et al. 2014) even though C. arcuata is its preferred host (Puttler et al. 2014). Even if E. klopomor seems to be the ideal candidate for a classical biological control program against OLB in Europe and western Asia, further research efforts are still unavoidable. There are numerous unanswered questions about the behavior and habitat of this parasitoid, so it needs to be studied both in the field and under laboratory conditions before it could be accepted as a biological control agent. As no other specialist natural enemy of OLB is known in its native range, E. klopomor seems to be the only candidate for the likely unavoidable classical biological control in the invaded range in the Palearctic region. Declarations Author Contribution Statement GC and MP conceived and designed research. GC, GM, MP and DB conducted sample collecting, ST validated collected specimens. GC, MP and ST analyzed data. GC and MP wrote the manuscript. All authors read and approved the manuscript. Acknowledgments For helping us out in the field, we would like to thank Warren and Chris Abrahamson, Matt Buffington, Eric Day, Kim Hoelmer, Sandy Liebhold, Gino Luzader, Carol Mapes, Laura Miller and Michael Joseph Skvarla. Funding Our research was funded from project ’K 142858’ implemented with the support of the Ministry of Innovation and Technology of Hungary from the National Research, Development and Innovation Fund, financed under the ’K22-OTKA’ funding scheme. Competing Interests The authors have no relevant financial or non-financial interests to disclose. Author Contributions György Csóka and Marton Paulin conceived and designed research. György Csóka, George Melika, Marton Paulin and David Bechtel conducted sample collection, Serguei Triapitsyn validated collected specimens. György Csóka, Marton Paulin and Serguei Triapitsyn analyzed data. György Csóka and Marton Paulin wrote the manuscript. All authors read and approved the final manuscript. 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(eds) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma . Prog Biol Control, vol 9. Springer, Dordrecht, 389–411 https://doi.org/10.1007/978-1-4020-9110-0_15 Mollot G, Pantel JH, Romanuk TN, (2017) The effects of invasive species on the decline in species richness: a global meta-analysis. In Adv Ecol Res 56, 61–83. https://doi.org/10.1016/bs.aecr.2016.10.002 Neimorovets VV, Shchurov VI, Bondarenko AS, Skvortsov MM, Konstantinov FV, (2017) First documented outbreak and new data on the distribution of Corythucha arcuata (Say, 1832) (Hemiptera: Tingidae) in Russia. Acta Zoologica Bulgarica, 9, 139–142. Nikolić N, Pilipović A, Drekić M, Kojić D, Poljaković-Pajnik L, Orlović S, Arsenov D, (2019) Physiological responses of pedunculate oak ( Quercus robur L.) to Corythucha arcuata (Say, 1832) attack. Arch Biol Sci, 71, 167–176. https://doi.org/10.2298/ABS180927058N Paulin M, Hirka A, Mikó Á, Tenorio-Baigorria I, Eötvös Cs, Gáspár Cs, Csóka Gy, (2020) A tölgy-csipkéspoloska Magyarországon – helyzetkép 2019 őszén [The oak-lace bug in Hungary - situation in the autumn of 2019]. Növényvédelem, 81 [N. S. 56]: 6, 245–250. Paulin M, Hirka A, Csepelényi M, Fürjes-Mikó Á, Tenorio-Baigorria I, Eötvös C, Gáspár C, Csóka G, (2021) Overwintering mortality of the oak lace bug ( Corythucha arcuata ) in Hungary–a field survey. Central European Forestry Journal, 67(2), 108–112. https://doi.org/10.2478/forj-2020-0024 Paulin MJ, Eötvös CB, Zabransky P, Csóka G, Schebeck M, (2023) Cold tolerance of the invasive oak lace bug, Corythucha arcuata . Agric Forest Entomol, 2023(1), 1–10. https://doi.org/10.1111/afe.12585 Peña J, E, Triapitsyn S, V, Long D, Evans G, A, Roltsch W, (2009) First Record of Erythmelus klopomor (Hymenoptera: Mymaridae) as a Parasitoid of the Avocado Lace Bug, Pseudacysta perseae (Heteroptera: Tingidae). Fla Entomol, 92(2), 394–395. https://doi.org/10.1653/024.092.0232 Puttler B, Triapitsyn SV, (2006) A new species of Anagrus (Hymenoptera: Mymaridae) from Missouri (USA), egg parasitoid of Corythucha marmorata (Hemiptera: Tingidae). Entomol News, 117(1), 25–30. https://doi.org/10.3157/0013-872X (2006)117[25:ANSOAH]2.0.CO;2 Puttler B, Bailey WC, Triapitsyn S, (2014) Notes on distribution, host associations, and bionomics of Erythmelus klopomor Triapitsyn (Hymenoptera, Mymaridae), an egg parasitoid of lace bugs in Missouri, USA, with particular reference to its primary host Corythucha arcuata (Say) (Hemiptera, Tingidae). Journal of Entomological and Acarological Research, 46(1), 30–34. https://doi.org/10.4081/jear.2014.1857 Roques A, (2010) Taxonomy, time and geographic patterns, in Roques A, Kenis M, Lees D, Lopez-Vaamonde C, Rabitsch W, Rasplus JY, Roy D, (eds), Alien terrestrial arthropods of Europe, 4 edition. BioRisk. Sofia, Bulgaria: Pensoft, 11–26. https://doi.org/10.3897/biorisk.4.70 Thunes KH, Søli GE, Thuróczy C, Fjellberg A, Olberg S, Roth S, Coulianos CC, Disney RHL, Starý J, Vierbergen G, Jonassen T, (2021) The arthropod fauna of oak ( Quercus spp., Fagaceae) canopies in Norway. Diversity, 13(7), 332. https://doi.org/10.3390/d13070332 Triapitsyn SV, Berezovskiy VV, Hoddle MS, Morse JG, (2007) A review of the Nearctic species of Erythmelus (Hymenoptera: Mymaridae), with a key and new additions to the New World fauna. Zootaxa, 1641, 1–64. Triapitsyn SV, Yasuhara Y, Adachi-Hagimori T, Tsukada M, (2024) Fairyfly egg parasitoids (Hymenoptera: Mymaridae) of the invasive lace bug Corythucha marmorata (Uhler) (Hemiptera: Tingidae) in Japan. J Asia-Pac Entomol, 27 (1), 102201 8. https://doi.org/10.1016/j.aspen.2024.102201 Yefremova ZA, Strakhova IS, (2010) A review of the species of the genus Elasmus Westwood (Hymenoptera, Eulophidae) from Russia and neighboring countries. Entomological Review 90, 903–926 (2010). https://doi.org/10.1134/S0013873810070080 Zhu CD, Huang DW, 2003: Preliminary Cladistics and Review of Hemiptarsenus Westwood and Sympiesis Förster (Hymenoptera: Eulophidae) in Hungary. Zoological Studies-Taipei, 42(2), 307–335. Additional Declarations No competing interests reported. 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PAULIN","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABB0lEQVRIiWNgGAWjYHACxgMJcHYFAwMbnCOBWw9UCzMQnyFWCwNMC2MbsjgOLebsZwwOPNzBEM0/+/zBx4XzDufxMbA/fFy4xyaPQbrHAJsWy54cgwOJZxhyZ5xLZjaeue1wMRsDj7HxjGdpxQwyZ7BqMTgA0tLGkNtwhplNmnfb4cQ2+Tds0jwHDic2SORg13L+DUTLfLCWOUAtDOzP8Gu5AbVlA1hLA0gLgxleLZYznhUAtUjkbjzDbGzMcywdqAXklwNpQMG0Aqwhxp+88eHPNpvceWcYHz7mqbFOnN8ADLGCAzaJ/RLJG7A6DEKhRQEoVpHiFKsWNMCMQ/UoGAWjYBSMTAAAHMNeNsu/0JQAAAAASUVORK5CYII=","orcid":"","institution":"University of Sopron","correspondingAuthor":true,"prefix":"","firstName":"MÁRTON","middleName":"J.","lastName":"PAULIN","suffix":""},{"id":400008176,"identity":"fcbe692f-6717-4f6e-96d0-040b249f5e10","order_by":1,"name":"GEORGE MELIKA","email":"","orcid":"","institution":"National Food Chain Safety Office","correspondingAuthor":false,"prefix":"","firstName":"GEORGE","middleName":"","lastName":"MELIKA","suffix":""},{"id":400008177,"identity":"3a445b3c-2f8a-4ea9-be21-73d8add6625f","order_by":2,"name":"SERGUEI TRIAPITSYN","email":"","orcid":"","institution":"University of California","correspondingAuthor":false,"prefix":"","firstName":"SERGUEI","middleName":"","lastName":"TRIAPITSYN","suffix":""},{"id":400008178,"identity":"3512dead-2f15-4a90-a28f-3956f1bb722a","order_by":3,"name":"DAVID BECHTEL","email":"","orcid":"","institution":"University of Tennessee","correspondingAuthor":false,"prefix":"","firstName":"DAVID","middleName":"","lastName":"BECHTEL","suffix":""},{"id":400008179,"identity":"8bbb49ea-06e5-4e44-ac0e-a6f661cd77e3","order_by":4,"name":"GYÖRGY CSÓKA","email":"","orcid":"","institution":"University of Sopron","correspondingAuthor":false,"prefix":"","firstName":"GYÖRGY","middleName":"","lastName":"CSÓKA","suffix":""}],"badges":[],"createdAt":"2025-01-09 10:54:00","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5795762/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5795762/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":73632372,"identity":"c4a33634-f532-4dbe-ae29-f940e02b9549","added_by":"auto","created_at":"2025-01-13 06:43:53","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":101749,"visible":true,"origin":"","legend":"\u003cp\u003eLocations of sampling sites\u003c/p\u003e","description":"","filename":"floatimage1.png","url":"https://assets-eu.researchsquare.com/files/rs-5795762/v1/5b7bcefe180cdcdc41ece9f4.png"},{"id":74368551,"identity":"7a1c7c8a-7077-4db3-a96d-042a1ea7833b","added_by":"auto","created_at":"2025-01-21 14:47:13","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":769122,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5795762/v1/ee0731aa-e8db-497c-965d-292a01c53672.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Erythmelus klopomor: First steps toward classical biological control of the oak lace bug Corythucha arcuata, a dangerous invader in the European oak forests","fulltext":[{"header":"Key Message","content":"\u003cp\u003e \u003cul\u003e \u003cli\u003e \u003cp\u003eThe invasive \u003cem\u003eCorythucha arcuata\u003c/em\u003e is a very dangerous pest of the European oak dominated forests\u003c/p\u003e \u003c/li\u003e \u003cli\u003e \u003cp\u003eNative enemies in Europe have no regulatory potential against \u003cem\u003eC. arcuata\u003c/em\u003e\u003c/p\u003e \u003c/li\u003e \u003cli\u003e \u003cp\u003eOnly a classical biological control program seems to be a feasible solution\u003c/p\u003e \u003c/li\u003e \u003cli\u003e \u003cp\u003eSo far \u003cem\u003eE. klopomor\u003c/em\u003e seems to be the only specialist parasitoid against \u003cem\u003eC. arcuata\u003c/em\u003e\u003c/p\u003e \u003c/li\u003e \u003c/ul\u003e \u003c/p\u003e"},{"header":"Introduction","content":"\u003cp\u003eAlien insect species can pose serious threats to various ecosystems worldwide (Roques 2010; Cs\u0026oacute;ka et al. 2017; Liebhold et al. 2017). While some of them do not have an evident impact on the newly colonized ecosystems, others may become invasive, rapidly expanding their range and imposing severe pressures on the novel habitats (Mollot et al. 2017; Blackburn et al. 2019; Haubrock et al. 2021). Whether a non-native species can become invasive is influenced by several intrinsic, species-specific traits as well as by external biotic and abiotic factors. An important, often appearing factor is the lack of regulatory effects by natural enemies; the so-called escape-from-enemy or enemy-release hypothesis (Brockerhoff et al. 2006; Brockerhoff \u0026amp; Liebhold 2017; Firlej et al. 2012).\u003c/p\u003e\n\u003cp\u003eThe North American oak lace bug (OLB), \u003cem\u003eCorythucha arcuata\u0026nbsp;\u003c/em\u003e(Say) (Hemiptera: Tingidae) was first found in Europe in northern Italy in 2000 (Bernardinelli 2000), and up to 2024 it was recorded in 24 European and 1 Asian countries (Paulin et al. 2023; Ciceu et al. 2024). Almost all Eurasian deciduous oak species are suitable hosts, and it can also feed on many other woody plants (Cs\u0026oacute;ka et al. 2019). More than 30 million hectares of oak forests in Europe provide suitable hosts for the OLB, meaning that the lack of suitable hosts will not restrict its further spread (Cs\u0026oacute;ka et al. 2019; Csepel\u0026eacute;nyi et al. 2017a; Paulin et al. 2020). OLB is also a typical \u0026ldquo;hitchhiker\u0026rdquo;, and its long-distance spread is supported by traffic. With this human-mediated help, it can overcome long distances and natural barriers within a short time. Also, after assessing the intensity of infestation on several pure and mixed oak stands in five countries, the conclusion was that mixed stands (while they mitigate OLB damage) do not prevent severe infestation (Hoch et al. 2024).\u003c/p\u003e\n\u003cp\u003eClimate may also have a very significant influence on the establishment, spread and population dynamics of an alien invasive species. Our field survey on the overwintering mortality (Csepel\u0026eacute;nyi et al. 2017b; Paulin et al. 2019) proved that the overwintering adults survived even relatively cold winters with ca. 50% or even less mortality. Lab experiments also proved that while OLB is a freeze-avoidant species, some adults may survive temperatures as low as -29\u0026deg;C (Paulin et al. 2021). Therefore, it is unlikely that low winter temperatures would significantly reduce spread of the OLB.\u003c/p\u003e\n\u003cp\u003eDetailed studies on the long-term impact of this species are not yet available but there are many good reasons to assume that it poses multiple threats to oaks and oak ecosystems (Paulin et al. 2020, Kern et al. 2021).\u003c/p\u003e\n\u003cp\u003eHeavy infestation of OLB on oaks may cause yellow-grey discoloration throughout the foliage by the second part of the vegetation season, sometimes even as early as late June (Csepel\u0026eacute;nyi et al. 2017a; Paulin et al. 2020). Drone, aerial and even space images (MODIS, Sentinel, Google Earth, etc.) have been used to detect severe infestations in several countries (Neimorovets et al. 2017; Kern et al. 2021). According to a Serbian study, the photosynthetic activity on heavily infested leaves decreased by 58.8% (Nikolić et al. 2019). Using MODIS data, the damage attributed to the OLB is also significant: NDVI decrease down to -14.5% in pure pedunculate oak forests (Kern et al 2021). It is very unlikely that such an impact would not have severe long-term effects on the oaks\u0026rsquo; nutrient and water flow. There is currently also no information on whether any oak pathogen present in these regions might potentially be vectored by OLB.\u003c/p\u003e\n\u003cp\u003eIt is yet unknown how several years of heavy OLB infestation will influence acorn crop, or what the effect on the oak herbivorous communities or other oak-associated species (like fungi or litter decomposers) will be. As the damage caused by OLB is more significant in the second half of the vegetation period, this influence can seriously harm oak specialist populations (Paulin et al 2020).\u003c/p\u003e\n\u003cp\u003eAdding to this, it was recorded of the closely related sycamore lace bug, \u003cem\u003eCorythucha ciliata\u0026nbsp;\u003c/em\u003e(Say), that their feeding attempts cause painful inflammations on human skin (Dutto \u0026amp; Bertero 2013; Izri et al. 2015). Similar results about OLB have not yet been documented, but our own experiences proved that OLB can cause similar symptoms (Paulin et al. 2020). This kind of human/OLB interaction will become more frequent in the future, especially in parks, oak alleys in towns and private gardens with planted oaks.\u003c/p\u003e\n\u003cp\u003eBased on current research results we found only a few species native in Europe which can be considered as occasional natural enemies of OLB. Most of the species recorded are generalists with negligible effect, such as \u003cem\u003eChrysoperla carnea\u0026nbsp;\u003c/em\u003e(Stephens) (Neuroptera: Chrysopidae), \u003cem\u003eHarmonia axyridis\u003c/em\u003e (Pallas) (Coleoptera: Coccinellidae) or \u003cem\u003eTheridion pinastri\u003c/em\u003e L. Koch (Araneae: Theridiidae) (Paulin et al. 2020). There are also records of entomopathogenic fungi naturally infecting overwintering OLB (Kovač et al. 2020). However, none of the above-mentioned native species have any significant controlling effect on OLB.\u003c/p\u003e\n\u003cp\u003eDuring 2019-2020, parasitoids of the invasive \u003cem\u003eC. arcuata\u003c/em\u003e were studied in Bulgaria (Georgiev et al. 2024). Larvae were collected from European oak (\u003cem\u003eQuercus\u003c/em\u003e \u003cem\u003erobur\u003c/em\u003e) and Turkey oak (\u003cem\u003eQuercus cerris\u003c/em\u003e) in five localities of the country. Five eulophid species (Hymenoptera: Eulophidae) were reported to be reared from the host larvae: \u003cem\u003eTamarixia pubescens\u0026nbsp;\u003c/em\u003e(Nees), \u003cem\u003eElasmus\u003c/em\u003e sp., \u003cem\u003eMinotetrastichus\u003c/em\u003e sp., \u003cem\u003ePnigalio\u003c/em\u003e sp. and \u003cem\u003eSympiesis\u003c/em\u003e sp. The impact of the parasitoids on the host number was reported to be very low (0.1-0.3%). However, \u003cem\u003eTamarixia pubescens\u003c/em\u003e is a parasitoid of psyllids (Hemiptera: Psylloidea); known to parasitize \u003cem\u003eTrioza remota\u003c/em\u003e (Foerster) (Triozidae), which, at nymphal stage, is an oak obligate (Thunes et al. 2021). \u003cem\u003eElasmus\u003c/em\u003e spp. most often were recorded as parasitoids of Lepidoptera (Yefremova and Strakhova 2010); and \u003cem\u003eMinotetrastichus\u003c/em\u003e sp., \u003cem\u003ePnigalio\u003c/em\u003e sp., \u003cem\u003eSympiesis\u003c/em\u003e sp. are known to parasitize various leaf miners (Boucek 1959; Zhu and Huang 2003; Japoshvili and Kostjukov 2017). Therefore, contamination of the samples (parasitoids emerging from other insects on or in the leaf samples in the rearing dishes) cannot be excluded, and, in fact, was almost certainly the case. Until proven otherwise by thorough experimental work, we do not consider these five species as being OLB parasitoids. In our opinion none of the native natural enemies (including pathogens) have any potential at regulating OLB in its invaded range in the Palearctic region.\u003c/p\u003e\n\u003cp\u003eTo control an insect pest, promising biological control candidates in its area of origin \u0026ndash; usually parasitoids \u0026ndash; often are chosen based on high observed parasitism levels (Hawkins et al. 1993). Such was the case with the chestnut gall wasp \u003cem\u003eDryocosmus kuriphilus\u003c/em\u003e Yasumatsu (Hymenoptera: Cynipidae) that has a strong negative effect on the growth of chestnut trees (Kato and Hijii 1997). A specialist parasitoid, \u003cem\u003eTorymus sinensis\u003c/em\u003e Kamijo (Hymenoptera: Torymidae), was introduced in multiple countries against this gall wasp (Ferracini et al. 2017). Post-release studies have found \u003cem\u003eT. sinensis\u0026nbsp;\u003c/em\u003eto be its effective biological control agent (Mato\u0026scaron;ević et al. 2016; Ferracini et al. 2017).\u003c/p\u003e\n\u003cp\u003eEgg parasitoids of Tingidae have been discovered in the past, mostly when their effects were of economic importance. Such cases were the parasitoids of the Chrysanthemum lace bug, \u003cem\u003eCorythucha marmorata\u0026nbsp;\u003c/em\u003e(Uhler) (Puttler \u0026amp; Triapitsyn 2006; Triapitsyn et al. 2024); the avocado lace bug, \u003cem\u003ePseudacysta perseae\u0026nbsp;\u003c/em\u003e(Heidemann) (Pe\u0026ntilde;a et al. 2009), and the OLB as well (Puttler et al. 2014). The subject of the latter was \u003cem\u003eErythmleus klopomor\u003c/em\u003e Triapitsyn (Hymenoptera: Mymaridae) which up to now is the only known parazitoid of OLB in its native range.\u0026nbsp;\u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003cp\u003eIn the first half of July 2023, we collected oak leaves with OLB egg bunches from 13 different locations in five states of the USA (Fig. 1., Table 1.). Leaves collected were first observed, and only further processed, if we estimated the percentage of unhatched eggs to be high enough (above 80%). Leaf parts with egg bunches were cut, producing approximately 2 cm-by-2 cm pieces. These were then put into transparent 25 ml containers, with a piece of paper tissue, held at room temperature, and checked every 1-3 days for emergence of either egg parasitoids or host nymphs.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eTable 1\u003c/em\u003e: Locations and dates of collection\u003c/p\u003e\n\u003cp\u003e\u003c/p\u003e\n\u003ctable border=\"0\" cellspacing=\"0\" cellpadding=\"0\" width=\"501\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eSite ID.\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 28.3433%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eLocation\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eLongitude\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eLatitude\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eDate of collection\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eNewark, DE\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e39.66227\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-75.75012\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.07\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eAllentown, PA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e40.61206\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-75.56745\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.08\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eKutztown, PA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e40.51368\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-75.78722\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.09\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eLewisburg, PA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e40.98655\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-76.93337\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.10\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003ePenn State U., PA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e40.91094\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-77.28275\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.12\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eMorgantown, WV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e40.80475\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-77.86446\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.13\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eGarards Fort, PA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e39.65119\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-79.98773\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.13\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eCoonskin Park, WV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e39.79613\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-80.09182\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.14\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eLittle Creek Park, WV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e38.38667\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-81.57509\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.15\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e10\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eVirginia Tech. U., VA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e38.34115\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-81.72315\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.16\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e11\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003ePandapas Pond, VA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e37.22500\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-80.42691\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.16\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e12\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eMcCormick Farm, VA\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e37.28206\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-80.46833\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.17\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\" style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e13\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eAgricultural RS, MD\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e37.93275\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\" style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-79.21297\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2023.07.18\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd style=\"width: 9.38124%;\"\u003e\n \u003cp\u003e14\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 28.3433%;\"\u003e\n \u003cp\u003eKnoxville, Tennessee\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 16.9661%;\"\u003e\n \u003cp\u003e35.85089\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 15.1697%;\"\u003e\n \u003cp\u003e-84.09388\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd style=\"width: 30.1397%;\"\u003e\n \u003cp\u003e2024.06.20.\u003c/p\u003e\n \u003cp\u003e2024.07.29.\u003c/p\u003e\n \u003cp\u003e2024.08.24.\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u003c/p\u003e\n\u003cp\u003eAnother separate sampling was done in Knoxville, Tennessee between 2024.06.20. and 2024.08.24. This collection will in later tables be identified as sample number 14. Samples were collected at three different times from the same tree and were processed in a similar way. If a large percentage of unhatched eggs was found, the leaf parts with egg bunches were cut. These were then put into transparent plastic Petri dishes with a piece of paper tissue and sealed using Parafilm.\u003c/p\u003e\n\u003cp\u003eUpon emergence, parasitoids emerged were collected and put into 2 ml Eppendorf tubes with 90% ethanol for later identification. Checking continued up to 39 days after collection. Individual eggs of bunches with parasitoids were also counted, to calculate parasitism rates for these samples. For the average rearing day count we used weighted arithmetic mean.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eOur initial observation was that collecting OLB eggs in the field proved to be more challenging than we first assumed. The abundance of OLB in its native range was magnitudes lower than what we have documented in Europe. On oaks that were in or close to natural habitats, we found only very few OLB-infested leaves. Our largest samples were collected in urban habitats or close to them, for example in university campuses or at roadsides. This supports our theory that one of the main factors for OLB\u0026rsquo;s success in its invaded range is the enemy free place. In our experience the \u0026lsquo;na\u0026iuml;ve host plant\u0026rsquo; theory doesn\u0026rsquo;t hold because as Cs\u0026oacute;ka et al. (2019) showed, that species from OLB\u0026rsquo;s native range were just as infected in the European sentinel gardens and arboreta, as in forests with European native oak species.\u003c/p\u003e\n\u003cp\u003eIn total during the two years of collecting, we visited 7 states in the USA, and from 14 locations we were able to collect a total of 423 individual egg masses, which contained above 95% unhatched eggs. Out of the 423 samples we have managed to rear parasitoids from 107 samples (Table 2). In the locations where the collected samples yielded no parasitoids, we were unable to collect more than 15 unhatched egg bunches.\u003c/p\u003e\n\u003cp\u003eIn the parasitized samples we counted 4569 oak lace bug eggs total, out of which we reared 721 parasitoids. The average mortality in the parasitized samples was between 3.6% and 18.3%, with the average of averages being 14.5%.\u0026nbsp;The average rearing day count (days between collecting and emergence) ranged from 8.6 to 24.6 days, with the average of averages being 19.5 days. It is important to remark, that these rearing days are most likely overestimates, as checking did not occur daily and sometimes only dead E. klopomor specimens were found.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eTable 2\u003c/em\u003e: Results of \u003cem\u003eErythmelus klopomor\u003c/em\u003e rearing (Abbreviations: ID.: Sample location ID from the previous table; SPL: Samples per location (pcs); SWP: Samples with parasitoids emerged (pcs); RP: Reared parasitoids in all samples (pcs); POLB: All OLB eggs in parasitised samples (pcs); ADTH: Avg. days to hatch after collecting; PSP: Percentage of samples parasitised; AEM: Avg. egg mortality in parasitized samples)\u003c/p\u003e\n\u003ctable border=\"0\" cellspacing=\"0\" cellpadding=\"0\" width=\"510\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003eID.\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eSPL\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eSWP\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eRP\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003ePOLB\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eADTH\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003ePSP\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eAEM\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e17\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e178\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e19.2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e8.2%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e9.6%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e16\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e78\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e284\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e20.6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e37.5%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e27.5%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e14\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e100\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e622\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e18.8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e28.6%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e16.1%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e38\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e40\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e358\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e14.3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e15.8%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e11.2%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e21\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e47\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e327\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e19.6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e33.3%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e14.4%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e16\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e15\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e86\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e11.0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e6.3%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e17.4%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e15\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e24\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e14\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e124\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e15.1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e16.7%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e11.3%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e34\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e12\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e331\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e19.4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e35.3%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e17.8%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e10\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e22\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e141\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e15.2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e9.1%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e3.6%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e11\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e0\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e12\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e22\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e36\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e8.8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e9.1%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e11.1%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e13\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e91\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e40\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e225\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e1443\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e18.9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e44.0%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e15.6%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e14\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e22\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e103\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e639\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e24.6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e40.9%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e18.0%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003eOverall\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e423\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e107\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e707\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e4569\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e19.5\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e23.7%\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"bottom\"\u003e\n \u003cp\u003e\u003cstrong\u003e14.5%\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003eEven though the number of 2024 samples from Tennessee was relatively low, it is still important to analyze them separately as they were collected on three different dates (Table 3). Nine out of 22 samples from there contained parasitoids. For these we compared the percentage of samples parasitized and the average egg mortality. The former shows an increase if we compare only the first two collecting dates; and the second shows an increase throughout all three collecting dates.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eTable 3:\u003c/em\u003e Results of \u003cem\u003eErythmelus klopomor\u003c/em\u003e rearing in Tennessee in 2024\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"519\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003eDate of collection\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003eSamples per location\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003eSamples with parasitoids emerged\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003ePercentage of samples parasitized\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003eAvg. egg mortality in parasitized samples\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e2024.06.20.\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e10\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e30.0%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e5.5%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e2024.07.29.\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e62.5%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e25.6%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e2024.08.24.\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e25.0%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e26.9%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u003cbr\u003e\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eEgg parasitoids, by definition, both attack and complete their development within a host egg (Mills 1994). The notion of killing a pest before it can hatch and cause significant damage to the host is appealing and is an important contributing factor for the usage of egg parasitoids in biological control and integrated pest management (Hassan 1993).\u003c/p\u003e\n\u003cp\u003eIn the context of classical biological control introductions, mymarid introductions have provided a number of spectacular results, and such opportunities should always be considered for new invasive pests, with particular emphasis on cicadellids and curculionids (Mills 2009). The success of augmentative biological control with egg parasitoids has been mixed, which highlights the need to know more about their ecology and behavior (Mills 2009). For example, to fully understand the impact that egg parasitoids have on host populations, all forms of parasitoid-induced mortality need to be considered \u0026ndash; for example, host eggs that have been parasitized, but from which neither parasitoids nor the hosts have emerged.\u003c/p\u003e\n\u003cp\u003eOur findings add five new states (Delaware, Pennsylvania, Tennessee, Virginia and West Virginia) in the USA to the previously known range of \u003cem\u003eE. klopomor\u003c/em\u003e. Puttler et al. (2014) reported it from Florida, Illinois, Missouri, North Carolina and Maryland. Although average temperature in these states is somewhat similar to temperature in the southern parts of Europe, there are plans to study distribution of this parasitoid in the northern regions of the United States.\u003c/p\u003e\n\u003cp\u003eIt is also important to acknowledge that most of our data is based on estimates. During the 2023 sampling we estimated the amount of unhatched OLB eggs in all samples to be above 80%, meaning there may have been eggs from which parasitoids could have already hatched. Also, in both years, after we completed rearing from the samples, we were unable to determine if there were any eggs (in any of the samples) which were unhatched. These eggs could have possibly contained \u003cem\u003eE. klopomor\u003c/em\u003e larvae, which were unable to develop for some reason. Therefore, both the percentage of parasitized samples and the average egg mortality caused by \u003cem\u003eE. klopomor\u0026nbsp;\u003c/em\u003ewere probably higher than what we have documented here.\u003c/p\u003e\n\u003cp\u003eAlthough the parasitism and mortality rates we documented seem to be low, it is important to note that most of these samplings were done in the first part of the vegetation period. Our theory (supported by our preliminary results) is that the rate of parasitism rises throughout the vegetative season, which is why it is capable of controlling OLB. The description of \u003cem\u003eE. klopomor\u0026rsquo;\u003c/em\u003es biology by Puttler et al. (2014) affirms this by reporting that the life cycle from egg to adult ranged from 11\u0026ndash;17 days. This means that its fast development enables it to \u0026ldquo;catch up\u0026rdquo; to the OLB\u0026rsquo;s multiple overlapping generations, and efficiently reduces the host\u0026rsquo;s numbers in the later months of the vegetation period.\u003c/p\u003e\n\u003cp\u003eFurther studies of this parasitoid are planned to understand its ecology better. We plan to study its overwintering habits, to ensure that it is capable of surviving in a novel environment. Studying host specificity and potential non-target effects is also a crucial point of this species\u0026rsquo; suitability as a classical biological control agent, especially considering that in its native range \u003cem\u003eE. klopomor\u0026nbsp;\u003c/em\u003ewas reported from several tingid species, mainly \u003cem\u003eCorythucha\u003c/em\u003e spp. (Triapitsyn et al. 2007; Pe\u0026ntilde;a et al. 2009; Puttler et al. 2014) even though \u003cem\u003eC. arcuata\u003c/em\u003e is its preferred host (Puttler et al. 2014).\u003c/p\u003e\n\u003cp\u003eEven if \u003cem\u003eE. klopomor\u003c/em\u003e seems to be the ideal candidate for a classical biological control program against OLB in Europe and western Asia, further research efforts are still unavoidable. There are numerous unanswered questions about the behavior and habitat of this parasitoid, so it needs to be studied both in the field and under laboratory conditions before it could be accepted as a biological control agent. As no other specialist natural enemy of OLB is known in its native range, \u003cem\u003eE. klopomor\u003c/em\u003e seems to be the only candidate for the likely unavoidable classical biological control in the invaded range in the Palearctic region.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003e\u003cu\u003eAuthor Contribution Statement\u003c/u\u003e\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eGC and MP conceived and designed research. GC, GM, MP and DB conducted sample collecting, ST validated collected specimens. GC, MP and ST analyzed data. GC and MP wrote the manuscript. All authors read and approved the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u003cu\u003eAcknowledgments\u003c/u\u003e\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eFor helping us out in the field, we would like to thank Warren and Chris Abrahamson, Matt Buffington, Eric Day, Kim Hoelmer, Sandy Liebhold, Gino Luzader, Carol Mapes, Laura Miller and Michael Joseph Skvarla.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eOur research was funded from project \u0026rsquo;K 142858\u0026rsquo; implemented with the support of the Ministry of Innovation and Technology of Hungary from the National Research, Development and Innovation Fund, financed under the \u0026rsquo;K22-OTKA\u0026rsquo; funding scheme.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial or non-financial interests to disclose.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eGy\u0026ouml;rgy Cs\u0026oacute;ka and Marton Paulin conceived and designed research. Gy\u0026ouml;rgy Cs\u0026oacute;ka, George Melika, Marton Paulin and David Bechtel conducted sample collection, Serguei Triapitsyn validated collected specimens. Gy\u0026ouml;rgy Cs\u0026oacute;ka, Marton Paulin and Serguei Triapitsyn analyzed data. Gy\u0026ouml;rgy Cs\u0026oacute;ka and Marton Paulin wrote the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData Availability\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets analyzed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eBernardinelli I (2000) Distribution of the Oak lace bug \u003cem\u003eCorythucha arcuata\u003c/em\u003e (Say) in northern Italy (Heteroptera Tingidae). 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Zoological Studies-Taipei, 42(2), 307\u0026ndash;335.\u003c/span\u003e\u003c/li\u003e \u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Oak lace bug, Erythmelus klopomor, Biological invasion, Classical biological control, Egg parasitoid","lastPublishedDoi":"10.21203/rs.3.rs-5795762/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5795762/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe North American oak lace bug (OLB), \u003cem\u003eCorythucha arcuata\u003c/em\u003e (Say, 1832) (Hemiptera: Tingidae), is a very dangerous invasive pest of European oaks (\u003cem\u003eQuercus\u003c/em\u003e spp., Fagaceae). It was first detected in Europe in 2000 and currently occurs in 26 countries in the Palearctic region. Most Eurasian deciduous oaks are suitable host plants, therefore about 30\u0026nbsp;million hectares of oak dominated forests in Europe can facilitate its rapid spread. Its negative effects can be very diverse: decreasing photosynthetic activity, deteriorating health, decreasing acorn yield, negative effect on other oak herbivorous insects, and more. One of the main reasons for its rapid expansion is that native European predators, parasitoids and insect pathogens are unable to control it. The only feasible control option is a classical biological control program, the essence of which is to find and introduce a preferably specialist regulatory species that is effective in the pest\u0026rsquo;s native range. In July 2023 and in 2024, we collected oak leaves with OLB eggs from different locations in six states of the United States of America. All emerged egg parasitoids were preserved for later identification. Our initial observation was that collecting OLB eggs in the field proved to be more challenging than we first assumed. Overall, 23.7% of the samples contained parasitoids, with the average parasitism of 14.5%. Up to this point results indicate that the fairyfly \u003cem\u003eErythmelus klopomor\u003c/em\u003e Triapitsyn, 2007 (Hymenoptera: Mymaridae) is the only known egg parasitoid of OLB. Its host range is restricted to lace bugs, mainly \u003cem\u003eCorythucha\u003c/em\u003e spp., and \u003cem\u003eC. arcuata\u003c/em\u003e seems to be its preferred host. Our conclusion is that E. \u003cem\u003eklopomor\u003c/em\u003e is a promising and only (at least so far) candidate for a classical biological control program, but further research efforts are unavoidable to clarify its life history parameters and minimize the risk of unintended non-target effects prior to a potential deliberate introduction to Europe.\u003c/p\u003e","manuscriptTitle":"Erythmelus klopomor: First steps toward classical biological control of the oak lace bug Corythucha arcuata, a dangerous invader in the European oak forests","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-01-13 06:27:48","doi":"10.21203/rs.3.rs-5795762/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"2669da4d-04e1-4dfd-9283-e11fe58050df","owner":[],"postedDate":"January 13th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2025-01-21T14:39:06+00:00","versionOfRecord":[],"versionCreatedAt":"2025-01-13 06:27:48","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5795762","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5795762","identity":"rs-5795762","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}